Protein Ser/Thr/Tyr Phosphorylation in the Archaea

Abstract

The third domain of life, the Archaea (formerly Archaebacteria), is populated by a physiologically diverse set of microorganisms, many of which reside at the ecological extremes of our global environment. Although ostensibly prokaryotic in morphology, the Archaea share much closer evolutionary ties with the Eukarya than with the superficially more similar Bacteria. Initial genomic, proteomic, and biochemical analyses have revealed the presence of "eukaryotic" protein kinases and phosphatases and an intriguing set of serine-, threonine-, and tyrosine-phosphorylated proteins in the Archaea that may offer new insights into this important regulatory mechanism. A Maturing Evolutionary Perspective on Protein (De)phosphorylationFor several decades, the phosphorylation of proteins on serine and threonine residues was generally regarded as exclusively eukaryotic in origin and distribution, an adaptation to the coordination and communication requirements of a more complex compartmentalized cell form (1). In this scenario, tyrosine phosphorylation emerged to meet the expanded signal transduction needs of "higher" eukaryotes composed of multiple differentiated cells. The persistence and pervasiveness of this viewpoint are manifested by the continued use of the designator "eukaryotic protein kinase" (ePK) 2 when referring to homologs of the prototype for this superfamily, the catalytic subunit of the cAMP-dependent protein kinase.As the 1990s dawned, occasional reports surfaced indicating the presence of eukaryotic protein kinases and protein phosphatases in bacteria and viruses (1, 2). However, their close association with pathogenic organisms, tendency to target proteins endogenous to their eukaryotic hosts, and frequent coding by mobile elements such as plasmids were consistent with acquisition from the Eukarya by lateral gene transfer. It was not until genomics fueled a quantum leap in our understanding of the macromolecular populations within living organisms that it became apparent that many ostensibly eukaryotic protein kinases and protein phosphatases were in fact indigenous to some prokaryotes as well (3, 4). Early Studies on Protein Phosphorylation in the ArchaeaIn the late 1970s, the Archaea emerged as a new player in the exploitation of phylogenetic diversity for tracing the evolution of biological macromolecules (5). Although morphologically prokaryotic, the rRNA sequences of the Archaea were more closely related to those of the Eukarya than to the superficially similar Bacteria, indicating that the first divergence from the last universal common ancestor separated the bacterial line of descent from a conjoint eukaryal/archaeal one.The first indication that archaeal proteins were subject to regulation via covalent phosphorylation was reported by Spudich and Stoeckenius (6), who detected multiple radiolabeled polypeptides in extracts from cultures of the extreme halophile Halobacterium halobium that were grown in media containing 32 P-labeled inorganic phosphate. The radiolabel remained associated with the poly...

Archaeal genome and cancerogenesis

“…A candidate for the direct lineal descendant of the primordial ePK, are found in archaea but absent in bacteria [19]. That means thet first divergence from the LUCA separated the bacterial line of descent from a conjoint eukaryal/archaeal one -primarly via direct inheritance.…”

Bacterial spore coat protein kinases: A new twist to an old story

“…Nowhere is this more apparent than in biology, where nature cleverly recycles and adapts the same chemical reactions to control complex physiology from bacteria to archaea, plants, and metazoans (1,2). However, those of us who work on protein phosphorylation have been lured into thinking bacteria do it one way and the rest of nature another.…”

In the Beginning, There Was Protein Phosphorylation

“…Indeed, the phosphoproteomes of archaea that have been examined contain phosphoSer, phospho-Thr, and phospho-Tyr. By contrast, the phosphatases in these organisms diverge structurally and fall into either the protein-Ser/Thr phosphatase or protein-Tyr phosphatase superfamily (15).…”

“…Still, it is important to note that the structural resemblance between eukaryotic and archaeal protein kinases and phosphatases suggests, as Kennelly notes, that the first eukaryotic protein kinases likely appeared after the divergence of the combined archaeal/eukaryotic line but prior to the divergence of the archaea from eukaryotes (15).…”

“…The stoichiometry of each phosphorylation event and its physiological significance are somewhat unclear; however, the sheer number of phosphoproteins in these archaea indicates relevance. Indeed, substantial alterations in the S. solfataricus phosphoproteome change with alterations in the nutrient milieu, and in vitro studies indicate that kinases in these organisms can regulate metabolic enzymes in a phosphorylation-dependent manner (15).…”